Dataset Information

On the value of nuclear and mitochondrial gene sequences for reconstructing the phylogeny of vanilloid orchids (Vanilloideae, Orchidaceae).

ABSTRACT:

Background and aims

Most molecular phylogenetic studies of Orchidaceae have relied heavily on DNA sequences from the plastid genome. Nuclear and mitochondrial loci have only been superficially examined for their systematic value. Since 40% of the genera within Vanilloideae are achlorophyllous mycoheterotrophs, this is an ideal group of orchids in which to evaluate non-plastid gene sequences.

Methods

Phylogenetic reconstructions for Vanilloideae were produced using independent and combined data from the nuclear 18S, 5.8S and 26S rDNA genes and the mitochondrial atpA gene and nad1b-c intron.

Key results

These new data indicate placements for genera such as Lecanorchis and Galeola, for which plastid gene sequences have been mostly unavailable. Nuclear and mitochondrial parsimony jackknife trees are congruent with each other and previously published trees based solely on plastid data. Because of high rates of sequence divergence among vanilloid orchids, even the short 5.8S rDNA gene provides impressive levels of resolution and support.

Conclusions

Orchid systematists are encouraged to sequence nuclear and mitochondrial gene regions along with the growing number of plastid loci available.

SUBMITTER: Cameron KM

PROVIDER: S-EPMC2720648 | biostudies-literature | 2009 Aug

REPOSITORIES: biostudies-literature

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Publications

On the value of nuclear and mitochondrial gene sequences for reconstructing the phylogeny of vanilloid orchids (Vanilloideae, Orchidaceae).

Cameron Kenneth M KM

Annals of botany 20090226 3

<h4>Background and aims</h4>Most molecular phylogenetic studies of Orchidaceae have relied heavily on DNA sequences from the plastid genome. Nuclear and mitochondrial loci have only been superficially examined for their systematic value. Since 40% of the genera within Vanilloideae are achlorophyllous mycoheterotrophs, this is an ideal group of orchids in which to evaluate non-plastid gene sequences.<h4>Methods</h4>Phylogenetic reconstructions for Vanilloideae were produced using independent and ...[more]

PMID: 19251715

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Project description:The Vanilloideae (vanilloids) is one of five subfamilies of Orchidaceae and is composed of fourteen genera and approximately 245 species. In this study, the six new chloroplast genomes (plastomes) of vanilloids (two Lecanorchis, two Pogonia, and two Vanilla species) were decoded, and then the evolutionary patterns of plastomes were compared to all available vanilloid plastomes. Pogonia japonica has the longest plastome, with 158,200 bp in genome size. In contrast, Lecanorchis japonica has the shortest plastome with 70,498 bp in genome size. The vanilloid plastomes have regular quadripartite structures, but the small single copy (SSC) region was drastically reduced. Two different tribes of Vanilloideae (Pogonieae and Vanilleae) showed different levels of SSC reductions. In addition, various gene losses were observed among the vanilloid plastomes. The photosynthetic vanilloids (Pogonia and Vanilla) showed signs of stage 1 degradation and had lost most of their ndh genes. The other three species (one Cyrotsia and two Lecanorchis), however, had stage 3 or stage 4 degradation and had lost almost all the genes in their plastomes, except for some housekeeping genes. The Vanilloideae were located between the Apostasioideae and Cypripedioideae in the maximum likelihood tree. A total of ten rearrangements were found among ten Vanilloideae plastomes when compared to the basal Apostasioideae plastomes. The four sub-regions of the single copy (SC) region shifted into an inverted repeat (IR) region, and the other four sub-regions of the IR region shifted into the SC regions. Both the synonymous (dS) and nonsynonymous (dN) substitution rates of IR in-cooperated SC sub-regions were decelerated, while the substitution rates of SC in-cooperated IR sub-regions were accelerated. A total of 20 protein-coding genes remained in mycoheterotrophic vanilloids. Almost all these protein genes show accelerated base substitution rates compared to the photosynthetic vanilloids. Two of the twenty genes in the mycoheterotrophic species faced strong "relaxed selection" pressure (p-value < 0.05).

Project description:In order to understand the evolution of the orchid plastome, we annotated and compared 124 complete plastomes of Orchidaceae representing all the major lineages in their structures, gene contents, gene rearrangements, and IR contractions/expansions. Forty-two of these plastomes were generated from the corresponding author's laboratory, and 24 plastomes-including nine genera (Amitostigma, Bulbophyllum, Dactylorhiza, Dipodium, Galearis, Gymnadenia, Hetaeria, Oreorchis, and Sedirea)-are new in this study. All orchid plastomes, except Aphyllorchis montana, Epipogium aphyllum, and Gastrodia elata, have a quadripartite structure consisting of a large single copy (LSC), two inverted repeats (IRs), and a small single copy (SSC) region. The IR region was completely lost in the A. montana and G. elata plastomes. The SSC is lost in the E. aphyllum plastome. The smallest plastome size was 19,047 bp, in E. roseum, and the largest plastome size was 178,131 bp, in Cypripedium formosanum. The small plastome sizes are primarily the result of gene losses associated with mycoheterotrophic habitats, while the large plastome sizes are due to the expansion of noncoding regions. The minimal number of common genes among orchid plastomes to maintain minimal plastome activity was 15, including the three subunits of rpl (14, 16, and 36), seven subunits of rps (2, 3, 4, 7, 8, 11, and 14), three subunits of rrn (5, 16, and 23), trnC-GCA, and clpP genes. Three stages of gene loss were observed among the orchid plastomes. The first was ndh gene loss, which is widespread in Apostasioideae, Vanilloideae, Cypripedioideae, and Epidendroideae, but rare in the Orchidoideae. The second stage was the loss of photosynthetic genes (atp, pet, psa, and psb) and rpo gene subunits, which are restricted to Aphyllorchis, Hetaeria, Hexalectris, and some species of Corallorhiza and Neottia. The third stage was gene loss related to prokaryotic gene expression (rpl, rps, trn, and others), which was observed in Epipogium, Gastrodia, Lecanorchis, and Rhizanthella. In addition, an intermediate stage between the second and third stage was observed in Cyrtosia (Vanilloideae). The majority of intron losses are associated with the loss of their corresponding genes. In some orchid taxa, however, introns have been lost in rpl16, rps16, and clpP(2) without their corresponding gene being lost. A total of 104 gene rearrangements were counted when comparing 116 orchid plastomes. Among them, many were concentrated near the IRa/b-SSC junction area. The plastome phylogeny of 124 orchid species confirmed the relationship of {Apostasioideae [Vanilloideae (Cypripedioideae (Orchidoideae, Epidendroideae))]} at the subfamily level and the phylogenetic relationships of 17 tribes were also established. Molecular clock analysis based on the whole plastome sequences suggested that Orchidaceae diverged from its sister family 99.2 mya, and the estimated divergence times of five subfamilies are as follows: Apostasioideae (79.91 mya), Vanilloideae (69.84 mya), Cypripedioideae (64.97 mya), Orchidoideae (59.16 mya), and Epidendroideae (59.16 mya). We also released the first nuclear ribosomal (nr) DNA unit (18S-ITS1-5.8S-ITS2-28S-NTS-ETS) sequences for the 42 species of Orchidaceae. Finally, the phylogenetic tree based on the nrDNA unit sequences is compared to the tree based on the 42 identical plastome sequences, and the differences between the two datasets are discussed in this paper.

Project description:IntroductionGaleola lindleyana is a mycoheterotrophic orchid belonging to the tribe Vanilleae within the subfamily Vanilloideae.MethodsIn this study, the G. lindleyana plastome was assembled and annotated, and compared with other Vanilleae orchids, revealing the evolutionary variations between the photoautotrophic and mycoheterotrophic plastomes.ResultsThe G. lindleyana plastome was found to include 32 protein-coding genes, 16 tRNA genes and four ribosomal RNA genes, including 11 pseudogenes. Almost all of the genes encoding photosynthesis have been lost physically or functionally, with the exception of six genes encoding ATP synthase and psaJ in photosystem I. The length of the G. lindleyana plastome has decreased to 100,749 bp, while still retaining its typical quadripartite structure. Compared with the photoautotrophic Vanilloideae plastomes, the inverted repeat (IR) regions and the large single copy (LSC) region of the mycoheterotrophic orchid's plastome have contracted, while the small single copy (SSC) region has expanded significantly. Moreover, the difference in length between the two ndhB genes was found to be 682 bp, with one of them spanning the IRb/SSC boundary. The Vanilloideae plastomes were varied in their structural organization, gene arrangement, and gene content. Even the Cyrtosia septentrionalis plastome which was found to be closest in length to the G. lindleyana plastome, differed in terms of its gene arrangement and gene content. In the LSC region, the psbA, psbK, atpA and psaB retained in the G. lindleyana plastome were missing in the C. septentrionalis plastome, while, the matK, rps16, and atpF were incomplete in the C. septentrionalis plastome, yet still complete in that of the G. lindleyana. Lastly, compared with the G. lindleyana plastome, a 15 kb region located in the SSC area between ndhB-rrn16S was found to be inverted in the C. septentrionalis plastome. These changes in gene content, gene arrangment and gene structure shed light on the polyphyletic evolution of photoautotrophic orchid plastomes to mycoheterotrophic orchid plastomes.DiscussionThus, this study's decoding of the mycoheterotrophic G. lindleyana plastome provides valuable resource data for future research and conservation of endangered orchids.

Dataset Information

On the value of nuclear and mitochondrial gene sequences for reconstructing the phylogeny of vanilloid orchids (Vanilloideae, Orchidaceae).

Background and aims

Methods

Key results

Conclusions

Publications

On the value of nuclear and mitochondrial gene sequences for reconstructing the phylogeny of vanilloid orchids (Vanilloideae, Orchidaceae).

Similar Datasets

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